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Lagged cells in alert monkey lateral geniculate nucleus

Published online by Cambridge University Press:  01 September 2008

ALAN B. SAUL
ALAN B. SAUL*
Affiliation:
Department of Ophthalmology, Medical College of Georgia, Augusta, Georgia
*
*Address correspondence and reprint requests to: Alan B. Saul, Department of Ophthalmology, Medical College of Georgia, Augusta, GA 30912. E-mail: asaul@mcg.edu
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Abstract

Five lagged cells were recognized by extracellular recording in the lateral geniculate nucleus of an awake, behaving macaque monkey. Previous reports of lagged cells were all in the anesthetized cat. Both parvocellular and magnocellular lagged cells were observed. Response timing was distributed continuously across the population, and both sustained and transient responses were seen in the magnocellular subpopulation. Cortex thus receives signals with a wide range of timing, which can mediate direction selectivity across multiple dimensions.

Keywords

Response timingMagnocellularParvocellularSustainedTransient
Type
Research Articles
Information
Visual Neuroscience , Volume 25 , Issue 5-6 , September 2008 , pp. 647 - 659
Copyright
Copyright © Cambridge University Press 2008

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References

Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284–299.CrossRefGoogle ScholarPubMed
Ahmad, A. & Spear, P.D. (1993). Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons. Journal of Comparative Neurology 334, 631–643.CrossRefGoogle ScholarPubMed
Alonso, J.-M., Usrey, W.M. & Reid, R.C. (2001). Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. Journal of Neuroscience 21, 4002–4015.CrossRefGoogle ScholarPubMed
Augustinaite, S. & Heggelund, P. (2007). Changes in firing pattern of lateral geniculate neurons caused by membrane potential dependent modulation of retinal input through NMDA receptors. Journal of Physiology 582, 297–315.CrossRefGoogle ScholarPubMed
Balercia, G., Kultas-Ilinsky, K., Bentivoglio, M. & Ilinksy, I.A. (1996). Neuronal and synaptic organization of the centromedian nucleus of the monkey thalamus: a quantitative ultrastructural study, with tract tracing and immunohistochemical observations. Journal of Neurocytology 25, 267–288.CrossRefGoogle ScholarPubMed
Blakemore, C. & Vital-Durand, F. (1986). Organization and post-natal development of the monkey’s lateral geniculate nucleus. Journal of Physiology 380, 453–491.CrossRefGoogle ScholarPubMed
Blitz, D.M. & Regehr, W.G. (2005). Timing and specificity of feed-forward inhibition within the LGN. Neuron 45, 917–928.CrossRefGoogle ScholarPubMed
Cai, D., DeAngelis, G.C. & Freeman, R.D. (1997). Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. Journal of Neurophysiology 78, 1045–1061.CrossRefGoogle ScholarPubMed
Conway, B.R. (2001). Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V1). Journal of Neuroscience 21, 2768–2783.CrossRefGoogle Scholar
Dacey, D.M & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.CrossRefGoogle ScholarPubMed
DeValois, R.L., Cottaris, N.P., Mahon, L.E., Elfar, S.D. & Wilson, J.A. (2000). Spatial and temporal receptive fields of geniculate and cortical cells and directional selectivity. Vision Research 40, 3685–3702.CrossRefGoogle Scholar
Dreher, B., Fukada, Y. & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates. Journal of Physiology 258, 433–452.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Peters, A. (1972). The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 144, 285–334.CrossRefGoogle ScholarPubMed
Ferrera, V.P., Nealey, T.A. & Maunsell, J.H.R. (1994). Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways. Journal of Neuroscience 14, 2080–2088.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. & Hawken, M.J. (1995). Temporal and chromatic properties of motion mechanisms. Vision Research 35, 1547–1563.CrossRefGoogle ScholarPubMed
Gonzalez, T. (1985). Clustering to minimize the maximum intercluster distance. Theoretical Computer Science 38, 293–306.CrossRefGoogle Scholar
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 128, 21–50.CrossRefGoogle ScholarPubMed
Gur, M. & Snodderly, D.M. (1987). Studying striate cortex neurons in behaving monkeys: Benefits of image stabilization. Vision Research 27, 2081–2087.CrossRefGoogle ScholarPubMed
Gur, M. & Snodderly, D.M. (2007). Direction selectivity in V1 of alert monkeys: Evidence for parallel pathways for motion processing. Journal of Physiology 585, 383–400.CrossRefGoogle ScholarPubMed
Hamori, J., Pasik, P. & Pasik, T. (1983). Differential frequency of P-cells and I-cells in magnocellular and parvocellular laminae of monkey lateral geniculate nucleus. An ultrastructural study. Experimental Brain Research 52, 57–66.CrossRefGoogle ScholarPubMed
Hamori, J., Pasik, P. & Pasik, T. (1991). Different types of synaptic triads in the monkey dorsal lateral geniculate nucleus. Journal für Hirnforschung 32, 369–379.Google ScholarPubMed
Hartveit, E. (1992). Simultaneous recording of lagged and nonlagged cells in the cat dorsal lateral geniculate nucleus. Experimental Brain Research 88, 229–232.CrossRefGoogle ScholarPubMed
Hartveit, E. & Heggelund, P. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. II. Non-lagged cells. Journal of Neurophysiology 63, 1361–1372.CrossRefGoogle Scholar
Hartveit, E. & Heggelund, P. (1992). The effect of contrast on the visual response of lagged and nonlagged cells in the cat lateral geniculate nucleus. Visual Neuroscience 9, 515–525.CrossRefGoogle ScholarPubMed
Hartveit, E. & Heggelund, P. (1993). Brain-stem influence on visual response of lagged and nonlagged cells in the cat lateral geniculate nucleus. Visual Neuroscience 10, 325–339.CrossRefGoogle ScholarPubMed
Hawken, M.J., Shapley, R.M. & Grosof, D.H. (1996). Temporal-frequency selectivity in monkey visual cortex. Visual Neuroscience 13, 477–492.CrossRefGoogle ScholarPubMed
Heggelund, P. & Hartveit, E. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. I. Lagged cells. Journal of Neurophysiology 63, 1347–1360.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Reid, R.C. (2000). The koniocellular pathway in primate vision. Annual Review of Neuroscience 23, 127–153.CrossRefGoogle ScholarPubMed
Horwitz, G.D., Chichilnisky, E.J. & Albright, T.D. (2005). Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1. Journal of Neurophysiology 93, 2263–2278.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Murthy, A. (1999). Cell types and response timings in the medial interlaminar nucleus and C-layers of the cat lateral geniculate nucleus. Visual Neuroscience 16, 513–525.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Saul, A.B. (1992). Action of brainstem reticular afferents on lagged and nonlagged cells in the lateral geniculate nucleus. Journal of Neurophysiology 68, 673–691.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Weller, R.E. (1988 a). Functionally distinct groups of X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 429–447.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Weller, R.E. (1988 b). Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 448–468.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125–143.CrossRefGoogle ScholarPubMed
Kultas-Ilinsky, K., Ribak, C.E., Peterson, G.M. & Oertel, W.H. (1985). A description of the GABAergic neurons and axon terminals in the motor nuclei of the cat thalamus. Journal of Neuroscience 5, 1346–1369.CrossRefGoogle ScholarPubMed
Kuroda, M., Sugiura, T., Shinkai, M., Murakami, K., Oda, S. & Kishi, K. (1993). Synaptic organization and prefrontal corticothalamic termination in the mediodorsal thalamic nucleus of the cat. Journal für Hirnforschung 34, 417–430.Google ScholarPubMed
Kwon, Y.H, Esguerra, M. & Sur, M. (1991). NMDA and non-NMDA receptors mediate visual responses of neurons in the cat’s lateral geniculate nucleus. Journal of Neurophysiology 66, 414–428.CrossRefGoogle ScholarPubMed
Kwon, Y.H., Nelson, S.B., Toth, L.J. & Sur, M. (1992). Effect of stimulus contrast and size on NMDA receptor activity in cat lateral geniculate nucleus. Journal of Neurophysiology 68, 182–196.CrossRefGoogle ScholarPubMed
Levitt, J.B., Schumer, R.A., Sherman, S.M., Spear, P.D. & Movshon, J.A. (2001). Visual response properties of neurons in the LGN of normally reared and visually deprived macaque monkeys. Journal of Neurophysiology 85, 2111–2129.CrossRefGoogle ScholarPubMed
Liu, S. & Wong-Riley, M. (1990). Quantitative light- and electron-microscopic analysis of cytochrome-oxidase distribution in neurons of the lateral geniculate nucleus of the adult monkey. Visual Neuroscience 4, 269–287.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Lu, S.M., Guido, W., Vaughan, J.W. & Sherman, S.M. (1995). Latency variability of responses to visual stimuli in cells of the cat’s lateral geniculate nucleus. Experimental Brain Research 105, 7–17.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. Journal of Comparative Neurology 161, 569–594.CrossRefGoogle ScholarPubMed
Malpeli, J.G., Schiller, P.H. & Colby, C.L. (1981). Response properties of single cells in monkey striate cortex during reversible inactivation of individual lateral geniculate laminae. Journal of Neurophysiology 46, 1102–1119.CrossRefGoogle ScholarPubMed
Marrocco, R.T. (1976). Sustained and transient cells in monkey lateral geniculate nucleus: Conduction velocities and response properties. Journal of Neurophysiology 39, 340–353.CrossRefGoogle ScholarPubMed
Martin, P.R., White, A.J.R., Goodchild, A.K., Wilder, H.D. & Sefton, A.E. (1997). Evidence that blue-ON cells are part of the third geniculocortical pathway in primates. European Journal of Neuroscience 9, 1536–1541.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1987 a). Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive field properties and classification of cells. Journal of Neurophysiology 57, 357–380.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1987 b). Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive field properties. Journal of Neurophysiology 57, 381–413.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1992). Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: receptive-field properties and retinal inputs. Visual Neuroscience 8, 407–441.CrossRefGoogle ScholarPubMed
Mastronarde, D.N., Humphrey, A.L. & Saul, A.B. (1991). Lagged Y cells in the cat lateral geniculate nucleus. Visual Neuroscience 7, 191–200.CrossRefGoogle ScholarPubMed
Merigan, W.H., Byrne, C.E. & Maunsell, J.H.R. (1991). Does primate motion perception depend on the magnocellular pathway? Journal of Neuroscience 11, 3422–3429.CrossRefGoogle ScholarPubMed
Minnery, B.S., Bruno, R.M. & Simons, D.J. (2003). Response transformation and receptive-field synthesis in the lemniscal trigeminothalamic circuit. Journal of Neurophysiology 90, 1556–1570.CrossRefGoogle ScholarPubMed
Montero, V.M. & Zempel, J. (1986). The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey. Experimental Brain Research 62, 215–223.CrossRefGoogle ScholarPubMed
Mullen, K.T. & Baker, C.L. Jr. (1985). A motion aftereffect from an isoluminant stimulus. Vision Research 25, 685–688.CrossRefGoogle ScholarPubMed
Mullen, K.T., Yoshizawa, T. & Baker, C.L. Jr. (2003). Luminance mechanisms mediate the motion of red-green isoluminant gratings: The role of “temporal chromatic aberration”. Vision Research 43, 1235–1247.CrossRefGoogle ScholarPubMed
Norden, J.J. & Kaas, J.H. (1978). The identification of relay neurons in the dorsal lateral geniculate nucleus of monkeys using horseradish peroxidase. Journal of Comparative Neurology 182, 707–725.CrossRefGoogle ScholarPubMed
O’Keefe, L.P., Levitt, J.B., Kiper, D.C., Shapley, R.M. & Movshon, J.A. (1998). Functional organization of owl monkey lateral geniculate nucleus and visual cortex. Journal of Neurophysiology 80, 594–609.CrossRefGoogle ScholarPubMed
Ralston, H.J. III & Ralston, D.D. (1994). Medial lemniscal and spinal projections to the macaque thalamus: an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms. Journal of Neuroscience 14, 2485–2502.CrossRefGoogle Scholar
Reichardt, W. (1959). Autocorrelation and the central nervous system. In Sensory Communication, ed. Rosenblith, A., pp. 303–318. Cambridge, MA: MIT Press.Google Scholar
Reid, R.C. & Shapley, R.M. (2002). Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. Journal of Neuroscience 22, 6158–6175.CrossRefGoogle ScholarPubMed
Reid, R.C., Victor, J.D. & Shapley, R.M. (1992). Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex. Visual Neuroscience 9, 39–45.CrossRefGoogle ScholarPubMed
Reitboeck, H.J. (1983). Fiber microelectrodes for electrophysiological recordings. Journal of Neuroscience Methods 8, 249–252.CrossRefGoogle ScholarPubMed
Ruppertsberg, A.I., Wuerger, S.M. & Bertamini, M. (2003). The chromatic input to global motion perception. Visual Neuroscience 20, 421–428.CrossRefGoogle ScholarPubMed
Sato, F., Nakamura, Y. & Shinoda, Y. (1996). Three-dimensional analysis of cerebellar terminals and their postsynaptic components in the ventral lateral nucleus of the cat thalamus. Journal of Comparative Neurology 371, 537–551.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Saul, A.B. (2008 a). Lagged cells. Neurosignals 16, 209–225.CrossRefGoogle ScholarPubMed
Saul, A.B. (2008 b). Temporal receptive field estimation using wavelets. Journal of Neuroscience Methods 168, 450–464.CrossRefGoogle ScholarPubMed
Saul, A.B., Carras, P.D. & Humphrey, A.L. (2005). Temporal properties of inputs to direction selective neurons in monkey V1. Journal of Neurophysiology 94, 282–294.CrossRefGoogle ScholarPubMed
Saul, A.B. & Feidler, J.C. (2002). Development of response timing and direction selectivity in cat visual thalamus and cortex. Journal of Neuroscience 22, 2945–2955.CrossRefGoogle ScholarPubMed
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and non-lagged cells in the cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206–224.CrossRefGoogle Scholar
Saul, A.B. & Humphrey, A.L. (1992 a). Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. Journal of Neurophysiology 68, 1190–1207.CrossRefGoogle ScholarPubMed
Saul, A.B. & Humphrey, A.L. (1992 b). Temporal frequency tuning of direction selectivity in cat visual cortex. Visual Neuroscience 8, 365–372.CrossRefGoogle ScholarPubMed
Schein, S.J. & deMonasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.CrossRefGoogle ScholarPubMed
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990). Functions of the colour-opponent and broad-band channels of the visual system. Nature 343, 68–70.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X- and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 475–477.CrossRefGoogle ScholarPubMed
Snodderly, D.M. & Gur, M. (1995). Organization of striate cortex (V1) of alert, trained monkeys (Macaca fascicularis): Ongoing activity, stimulus selectivity, and widths of receptive field activating regions. Journal of Neurophysiology 74, 2100–2125.CrossRefGoogle ScholarPubMed
Spear, P.D., Moore, R.J., Kim, C.B., Xue, J.T. & Tumosa, N. (1994). Effects of aging on the primate visual system: Spatial and temporal processing by lateral geniculate neurons in young adult and old rhesus monkeys. Journal of Neurophysiology 72, 402–420.CrossRefGoogle ScholarPubMed
Steriade, M., Paré, D., Hu, B. & Deschenes, M. (1990). The visual thalamocortical system and its modulation by the brain stem core. In Progress in Sensory Physiology, Vol. 10, ed. Ottoson, D.Berlin, Germany: Springer-Verlag.Google Scholar
Stockman, A. & Sharpe, L.T. (2000). The spectral sensitivities of the middle- and long-wavelength cones derived from measurements in observers of known genotype. Vision Research 40, 1711–1737.CrossRefGoogle ScholarPubMed
Stone, J. (1973). Sampling properties of microelectrodes assessed in the cat's retina. Journal of Neurophysiology, 36, 1071–1079.CrossRefGoogle ScholarPubMed
Szmajda, B.A., Buzás, P., Fitzgibbon, T. & Martin, P.R. (2006). Geniculocortical relay of blue-off signals in the primate visual system. Proceedings of the National Academy of Science United States of America 103, 19512–19517.CrossRefGoogle ScholarPubMed
Tang, Y., Saul, A.B., Gur, M., Goei, S., Wong, E., Ersoy, B. & Snodderly, D.M. (2007). Eye position compensation improves estimates of response magnitude and receptive field geometry in alert monkeys. Journal of Neurophysiology 97, 3439–3448.CrossRefGoogle ScholarPubMed
Towe, A.L. & Harding, G.W. (1970). Extracellular microelectrode sampling bias. Experimental Neurology 29, 366–381.CrossRefGoogle ScholarPubMed
van Santen, J.P.H. & Sperling, G. (1985). Elaborated Reichardt detectors. Journal of the Optical Society of America A 2, 300–321.CrossRefGoogle ScholarPubMed
Wang, C., Dreher, B. & Burke, W. (1994). Non-dominant suppression in the lateral geniculate nucleus of the cat: Laminar differences and class specificity. Experimental Brain Research 97, 451–465.CrossRefGoogle ScholarPubMed
Wang, C., Dreher, B. & Burke, W. (1996). Effects of eliminating retinal Y cell input on center-surround interactions in the dorsal lateral geniculate nucleus of the cat. Visual Neuroscience 13, 1089–1097.CrossRefGoogle ScholarPubMed
Watson, A.B. & Ahumada, A.J. Jr. (1985). Model of human visual-motion sensing. Journal of the Optical Society of America A 2, 322–342.CrossRefGoogle ScholarPubMed
Weber, A.J., Chen, H., Hubbard, W.C. & Kaufman, P.L. (2000). Experimental glaucoma and cell size, density, and number in the primate lateral geniculate nucleus. Investigative Ophthalmology and Visual Science 41, 1370–1379.Google ScholarPubMed
Wilson, J.R. (1989). Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. Journal of Neuroscience 9, 2931–3953.CrossRefGoogle ScholarPubMed
Winer, J.A., Miller, L.M., Lee, C.C. & Schreiner, C.E. (2005). Auditory thalamocortical transformation: Structure and function. Trends in Neuroscience 28, 255–263.CrossRefGoogle ScholarPubMed
Winfield, D.A. (1980). The synaptic organization of glomeruli in the magnocellular and parvocellular laminae of the lateral geniculate nucleus in the monkey. Brain Research 198, 55–62.CrossRefGoogle ScholarPubMed
Wolfe, J. & Palmer, L.A. (1998). Temporal diversity in the lateral geniculate nucleus of cat. Visual Neuroscience 15, 653–675.CrossRefGoogle ScholarPubMed
Xu, X., Ichida, J.M., Allison, J.D., Boyd, J.D. & Bonds, A.B. (2001). A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Journal of Physiology 531, 203–218.CrossRefGoogle ScholarPubMed